Associations of morphological changes in skeletal muscle with physical activity in preschool children

doi:10.21203/rs.3.rs-2067774/v1

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Associations of morphological changes in skeletal muscle with physical activity in preschool children

https://doi.org/10.21203/rs.3.rs-2067774/v1

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Background：Physical activity (PA) is likely to be the most important modifiable factor in skeletal muscle development. However, the influence of PA on skeletal muscle of preschool children has not been thoroughly investigated. The main objective of this study is to objectively measure PA) and then evaluate the association between site-specific muscle changes and PA in relation to sex and weight statusin preschool children aged 3 to 4 years.

Methods: A total of 86 healthy preschool children, aged 3-4 years, were instructed to wear an accelerometer for seven consecutive days. The number of steps taken daily and minutes spent in moderate-to-vigorous PA (MVPA) and total PA (TPA) were recorded. Muscle thickness was measured by B-mode ultrasonography using a 5-18 MHz scanning head. muscle thickness was measured at seven sites: the lateral forearm, upper arm, abdomen, anterior and posterior thigh, anterior and posterior lower leg.

Results: There was no significant difference between boys and girls in terms of MVPA and TPA on weekdays and weekends. According to the linear regression models, after adjusting for daylight duration, the muscle of the posterior thigh was significantly positively associated (p < 0.05) with daily steps and MVPA on weekdays for boys and girls, respectively.

Conclusions: We found that the muscle thickness of the posterior thigh in preschool children was significantly positively associated with PA, as measured by daily steps and MVPA. We suggest that for the overall health and wellbeing of preschool children, levels of PA should be maintained and/or increased, and preferably transformed into a regular part of daily living.

Physical fitness

Physical activity

Growth and development

Muscle growth

Skeletal muscle

Childhood is a key period for skeletal growth; body increases in size, and notably, changes in the proportions of muscle and fat mass are influenced by gender.[1]. Previous studies have reported differences in skeletal muscle and fat mass in children [2]. However, evaluation of results of muscle thickness of the forearm, thigh, and lower leg showed no significant sex difference in children and adolescents aged 0–18 years [3, 4]. It is difficult to measure skeletal muscle thickness in children and adolescents, partly because the site of examinable skeletal muscle can only be located in the upper or lower limbs.

Skeletal muscle is highly plastic and is capable of responding to a variety of stimuli [5, 6]. Several studies have reported that daily PA provides an important stimulus to the musculoskeletal system, which can improve muscle development. Some studies have suggested that children and adolescents with higher fat mass have lower than expected daily PA and are at an increased risk of fractures [7, 8]. Growing evidence suggests that daily PA in children and adolescents is negatively associated with total body fat [9]. Therefore, additional studies are needed to better understand the association between daily PA level and percentage body fat, which will provide useful insights for interventional studies that focus on enhancing daily PA and reducing percentage body fat in in the target group.

Recent research show that reduced PA levels are a strong predictor of weight gain and/or obesity in children and are associated with the risk of Cardiovascular disease factors [10, 11]. In addition, the role of muscle thickness has been increasingly recognized in the prevention of chronic disease in adults [12], and features of metabolic syndrome have been negatively associated with percentage body fat in men [13] and women [14]. Obesity is associated with an increase in muscle mass [15], suggesting that the strength production capacity of obese individuals is higher than that of non-obese participants. However, because obesity is also associated with a decrease in muscle quality [16, 17], the muscle gain yielded may eventually be of too poor quality to offset the increase in body fat percentage associated with reduced PA [18]. It is important to understand whether the relationship between PA and muscle thickness identified in children is independently related to the weight status in children, in order for effective evidence-based prevention and treatment strategies to be implemented as early as possible.

We previously reported that the quantity and intensity of PA is predominantly related to weight status in children [19], but it is unclear whether preschool children are also associated with PA and skeletal muscle. Therefore, further studies would be beneficial to determine whether daily PA and/or muscle thickness could be proposed as health markers at these ages. In view of the above, the main objectives of this study were to:

Evaluate the skeletal muscle thickness and objectively measure PA,

Determine the association between site-specific muscle thickness and level of PA with regard to sex and weight status in preschool children aged 3 to 4 years.

Participants

A total of 113 healthy preschool children, aged 3–5 years were selected, with selection criteria for admission into the study being: attendance of a preschool, permission from parents to participate in this study, and no injuries or current illnesses reported. The subjects’ parents provided informed consent in line with research protocol adhering to the Declaration of Helsinki, which was approved by the ethics committee of Juntendo University (No.29 − 17).

Anthropometrics Data

In 2017, all anthropometric data were collected by trained staff under the supervision of a school nurse. body mass, wearing only minimal clothing, was measured on a digital balance to the nears 0.1kg, and height was measured on a stadiometer to the nearest 0.1cm. BMI (kg/m²) was calculated as body weight/height squared. Weight status (i.e., underweight, normal weight and overweight/obese) was determined according to the age- and sex-specific cutoffs of the Working Group on Obesity in China (WGOC) [20]. Table 1 describes BMI standard cutoff criteria for the overweight and obese classification for preschool children in China.

---Insert Table 1 here---

Muscle Thickness

Muscle thickness (MTs) and fat thickness (FTs) were measured via B-mode ultrasonography using a 5–18 MHz scanning head (Noblus; Hitachi, Tokyo, Japan). The scanning head was prepared using a water-soluble transmission gel that provided acoustic contact without depressing the skin surface. MTs and FTs were obtained at seven sites on the anterior and posterior surface of the body [22]. The seven anatomical landmarks for the chosen sites were defined as follows: the upper arm (UA) site was approximately 60% distal to the entire upper arm between the lateral epicondyle of the humerus near the elbow and the acromial process of the scapula at the shoulder; the forearm (FA) site was on the anterior surface, 30% proximal between the styloid process of the wrist and the head of the radius at the elbow; the abdominal (AB) site was at a distance of 3 cm to the right of the umbilicus; the anterior thigh (AT) and posterior thigh (PT) sites were on the anterior and posterior surfaces of the upper leg, midway between the lateral condyle of the femur at the knee and the greater trochanter at the hip; and lastly anterior (AL) and posterior (PL) lower leg sites were approximately 30% proximal to the talus between the lateral malleolus of the fibula at the ankle and the lateral condyle of the tibia at the knee.

Physical Activity

We measured PA using a uniaxial Kenz GS AC (Lifecorder, Suzuken Co., Ltd, Nagoya, Japan; 60 g). Each child attached the accelerometer (AC) to their waist and wore it from the time they got up in the morning, until they went to bed. They were instructed to wear the AC from Monday to Sunday, providing seven consecutive days of data. The accelerometer has been previously validated in the study of children and adolescents[23, 24]. According to the scale, distinctions were made regarding intensity (levels 1–3, 4–6, and 7–9), where light PA (LPA) was defined as AC intensity levels of 1–3 and 1.5–2.9 metabolic equivalent of task; moderate PA (MPA), AC intensity levels of 4–6 and 3.0-5.9 METs; and vigorous PA (VPA), AC intensity levels of 7–9 and ≥ 6.0 METs[25, 26]. We recorded crude step counts to estimate activity levels, and the time spent in MVPA (≥ 3.0 METs) was calculated as the sum of the MPA and VPA minutes, and TPA = LPA + MPA + VPA for each day. The study required at least four days of recording (including weekends), with a minimum of 10-hour of wear time per day, for inclusion in the subsequent analysis[27]. We excluded days when no signal was detected for more than one hour by the AC, and this period was regarded as non-wearing time.

Data analysis

The results are presented as mean deviation and standard deviation (SD). We conducted a two-way analysis of variance (ANOVA) to determine the variability in each muscle thickness and daily PA outcome (steps, MVPA, and TPA) among the sexes, and weight status. A 2 (sex: boys and girls) × 2 (weight status: normal and overweight/obese) ANOVA was used to assess variability during weekdays and weekends. ANOVA with Bonferroni post-hoc test was used to determine their significance.

To determine the bivariate relationships between all indicators of muscle thickness and daily PA, we conducted linear regression models (reported as Pearson's correlation coefficients) by inserting all indicators of muscle thickness as independent variables and daily PA as dependent variable. Two models were used in this study. Model 1 was an unadjusted analysis of the muscle thickness and PA. Model 2 was adjusted for height, weight, and duration of daylight. There was no interaction noted between month age groups and the outcomes of PA, which indicates that the pattern of the association with muscle thickness and daily PA was similar in 3- and 4-year-old preschool children. Therefore, the analysis grouped children aged three and four years old together and included month age as a covariate in the model.

Statistical analysis was conducted using SPSS software (version 22.0; SPSS Inc., IBM, USA), and the level of significance was set at p < 0.05.

Participant characteristics

A total of 86 preschool children (47 boys and 39 girls) met the inclusion criteria and were included in the analyses (Table 2). For preschool children, the median age was 49 ± 6 months for boys and girls, as shown in Table 2. Boys and girls had similar physical characteristics. Of the study population, 13.8% of the boys and 8.6% of the girls were classified as overweight or obese according to the WGOC thresholds of BMI. As shown in Table 2, boys and girls in the weight status groups had significantly higher weights and BMI than those in the NW group (p < 0.05).

---Insert Table 2 here---

Muscle Thickness And Fat Thickness Values (Table 3)

Descriptive characteristics and ultrasound MTs measurements of preschool children in relation to sex and weight status are reported in Table 3. Girls had significantly lower muscle thickness of the UA, FA, and AL than boys. For boys, the OW/OB group had significantly greater thickness of UA, FA, AT, PT, AL, and PL than those in the NW group (p < 0.05). For girls, the OW/OB group had significantly greater FA, AT, PT, AL, and PL thickness.

All indicators of fat thickness values were significantly higher in girls than in boys as well as in the OW/OB group compared to their NW peers (p < 0.05).

---Insert Table 3 here---

Daily Physical Activity Outcomes (Table 4)

There was no significant difference between boys and girls in steps, MVPA, and TPA, except for TPA on weekends (girls were significantly less active than boys [107.8 min ± 22.4 vs. 124.0 min ± 24.4, p < 0.05]).

According to weight status, no significant differences were found in steps, MVPA, and TPA between the NW and OW/OB groups on both weekdays and weekends in either boys or girls.

---Insert Table 4 here---

Association Between Muscle Thickness And Fat Thickness Values In Line With Physical Activity

Table 5 presents the results of the linear regression models. For boys, the AB muscle was positively associated with daily steps and MVPA on weekdays. The PT muscle was positively associated with steps on both weekdays and weekends, and MVPA on weekends (p < 0.05). Regarding fat thickness, only FA was negatively associated with MVPA on weekdays (p < 0.05).

In girls, the PT and PL muscles were positively associated with daily steps, MVPA, and TPA on weekends. With regards to fat thickness, PT was negatively associated with daily steps and MVPA on weekdays, whereas PL was negatively associated with MVPA on weekdays (p < 0.05).

The adjusted associations between muscle thickness and fat thickness with PA for each characteristic measurement are shown in Table 6. In the adjusted analyses, the most consistent results were established for the PT muscle, which was significantly positively associated with daily steps and MVPA on weekday and TPA on both weekdays and weekends. Moreover, the fat thickness of the UA was negatively associated with daily steps, MVPA, and TPA on weekdays in boys (p < 0.05).

For girls, in the adjusted analyses, the most consistent results were established for the PT and PL muscles, which were significantly positively associated with daily steps and MVPA on weekdays, and MVPA on weekends, respectively. Moreover, AB was positively associated with all PA outcomes on weekdays and weekends. For fat thickness, PT and PL were inversely associated with daily steps and MVPA on weekdays, independent of covariates, respectively (p < 0.05).

---Insert Tables 5 and 6 here---

This study examined the association between muscle thickness and PA with the weight status of Chinese preschool children after adjusting for several potential confounding factors. These findings expand the current literature since this is, to the best of our knowledge, the first study to report an association between measures of muscle thickness and PA in preschoolers in China. Our data showed that muscle thickness of preschool children had significant positive associations with PA, both in daily steps and MVPA. The relationships were stronger for the lower legs than for the arms, and for girls than for boys.

In this study, after adjustments for month-age, height, and weight, we observed that the relationships of muscle thickness of the lower limb were positively associated with daily steps and MVPA on weekdays for boys. Similar relationships were also observed in the AB muscle, and the lower limb was positively associated with daily steps and MVPA on both weekdays and weekends for girls. These results suggest that decreasing muscle thickness and increasing fat thickness in early childhood (OW/OB) may affect fitness performance and PA.

Our results indicated that the positive associations between muscle thickness and the objective measurements of PA, especially moderate and vigorous intensity, were correlated more strongly with lower limb muscle mass than with upper limb muscle mass. Few studies have investigated the association between muscle thickness and PA according to weight status in preschool children. There is some evidence that showed a significantly positive relationship between walking speed and knee extension torque with both daily steps and intensity of activity > 3 METs [28]. These observations may indicate a causal relationship, since walking, the primary component of our indices of habitual activity, is more likely to maintain muscle function in the legs than in the arm [29]. Furthermore, our observed associations remained statistically significant for objectively measured PA levels after adjusting for several potential confounding factors. A recent meta-analysis examining PA and metabolic outcomes found that a 10-min increase in MVPA was associated with a smaller waist circumference and lower fasting insulin levels [30]. To our knowledge, no previous study has reported an association between muscle thickness and PA in preschool children. Thus, in the present study, the lack of daily steps and MVPA may be major contributing factors to the increasing prevalence of overweight or obesity in children.

Our findings showed a significant effect of sex on all indicators of fat thickness, but no difference in muscle thickness. Cross-sectional studies have demonstrated similar sex differences in muscle thickness between boys and girls aged 3–18 years [31], although the differences were only observed in the upper arm. In Western countries, the percentage body fat rate rapidly increases to 25% one year after birth, then decreasing around the age of 5 years. As girls begin to increase percentage body fat around the age of 6 years, and then continue to increase until adulthood. Boys, however, only begin to increase their percentage body fat from the age of 7 years and peak at 11 years old, after which a decrease is observed due to the rapid increase in fat-free mass [32]. Thus, our results confirm those of prior studies [33, 34] demonstrating that boys had significantly less body fat than girls. In contrast, boys had significantly higher muscle thickness than girls in some ranges, as demonstrated in this study. No obvious sex differences in BMI was observed in our study between boys and girls, which has previously been found in other studies. [34] The sex-specific pattern of fat accumulation during childhood was characterized by a steady increase of subcutaneous fat accumulation in girls. From these considerations, it was shown that sex differences do exist in the fat thickness of the upper and lower limbs from infancy to early childhood.

Our results also revealed no significant differences in PA between weekdays and weekends among NW and OW/OB children in these age groups, although the intensity level of PA was higher in the group of preschool children who were not overweight/obese. Similar data were presented in a Portuguese study with preschool children of equivalent age [35]. In contrast, several studies performed in older children (> 6 years) showed a close and significant inverse relationship between weight status and PA in overweight and obese children, with significantly less PA than in their normal-weight peers [19, 36]. Extending these findings in children, a recent study revealed a close relationship between percentage body fat and the level of PA, measured as steps per day, and MVPA in both sexes of children aged 8, 10, and 12 years [37]. The fact that we did not find a correlation between weight status and daily PA in preschool children leads us to conclude that, in younger children, the natural drive to be active is not influenced by a higher BMI, as it seems to be in old children. Therefore, it is essential to initiate preventive interventions in this age group. The urgent need for early intervention is underlined by the fact that PA seems to decrease from childhood to adolescence. As there are no validated obesity prevention strategies for childhood and adolescence, early identification of potential risk factors is crucial. In adults, the level of PA may predict the risk of developing chronic diseases in the future. However, our results suggest that risk prediction for obesity and associated diseases may not be assumed by PA in preschool children, but PA may be of increasing importance during the course of childhood development [38]. Thus, promotion of PA that starts as early as possible may prevent chronic diseases later in life.

According to sex and day of the week (weekdays and weekends), this study did not identify differences in PA between sex and day of the week. This is consistent with some [39, 40] but not all previous studies [41, 42]. Previous research has suggested that the differences in sex and day of the week might be explained by the fact that preschool children's PA is not more influenced by the environment, but rather by personal factors [39]. Rowlands et al [43] found a drop in PA in children aged 9 to 11 years during weekends. These findings suggest that the tendency of children to be less active during weekends begins at a very young age, which might require special attention in future activity interventions. Moreover, we also believe that issues such as the involvement of family and the perception of an unfavorable family environment, together with social roles for girls, may play a role in why children are less active [44] over the weekend.

This study has some limitations. Owing to the cross-sectional design of the study, causality and direction of associations cannot be concluded. Furthermore, the study included preschool children from a large metropolitan area, which makes it difficult to generalize these findings. Although we controlled for several potential confounders, such as age, height, and weight, we cannot be certain that other unmeasured confounders, such as dietary intake or genetic variation, did not have an influence on our findings. Therefore, future studies should address these issues.

In conclusion, our study demonstrated that higher muscle and lower fat thickness were associated with higher levels of PA, especially MVPA. The findings also suggest that preschool children seem to be engaging adequately in PA. Developing health habits at this early stage increases the probability of these habits continuing into later life. It may be as important to maintain and/or increase the amount of PA in preschool children as it is to foster awareness of the importance of PA and transform it into a regular daily habit.

PA: Physical Activity; total PA (TPA); MVPA: Moderate-vigorous Physical Activity; light PA (LPA); moderate PA (MPA); vigorous PA (VPA); accelerometer (AC); BMI: Body Mass Index; Muscle thickness [21]; Fat thickness (FTs); upper arm (UA); forearm (FA) abdominal (AB); anterior thigh (AT); posterior thigh (PT); anterior lower leg (AL); posterior lower leg (PL)

Ethics approval and consent to participate

The study was approved by the Research Ethics Committee of Juntendo University (No.29-17) on July 10 2017 and the participants confidentiality was strictly maintained throughout the study. No potential conflicts of interest were declared as well written study information and informed consent forms were sent to the participants parents by the study team. In addition, teachers in each kindergarten received the study introduction comment. The children were faunally included in the study when the informed consent forms were received.

Consent for publication

Not applicable

Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that the have no competing interests.

Funding

This work was supported by JSPS KAKENHI Grant Number 16H07183 and 20K19610, the Juntendo University Japanese Center for Research on Women in Sport and the Juntendo University Institute of Health and Sports Science & Medicine. The experiments comply with the current laws of the country in which they were performed.

Authors’ contributions

PD performed the drafted the manuscript, data interpretation and statistical analysis. HO, TN and DK conceived of the study, participated in its design and helped to draft the manuscript. DL, KS and HN participated in the design and revised the manuscript. All authors read and approved the final manuscript.

Acknowledgements

Children and participating kindergarten.

Author details

¹ School of Health and Sports Science, Juntendo University, Inzai, Chiba, Japan. ² Graduate School of Health and Sports Science, Juntendo University, Inzai, Chiba, Japan. ³ School of Sport and Health Science, Tokai Gakuen University, Miyoshi, Japan. ⁴ Department of Human Structure & Function, Tokai University School of Medicine, 143 Shimokasuya, Iesehara, Kanagawa, 259-1193, Japan. ⁵ School of Public Health, Fudan University, Shanghai, China. 6 School of Kinesiology, Shanghai University of Sport, Shanghai, China.

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Tables 1 to 6 are available in the Supplementary Files section

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Associations of morphological changes in skeletal muscle with physical activity in preschool children

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Abstract

Background

Methods

Participants

Anthropometrics Data

Muscle Thickness

Physical Activity

Data analysis

Results

Participant characteristics

Muscle Thickness And Fat Thickness Values (Table 3)

Daily Physical Activity Outcomes (Table 4)

Association Between Muscle Thickness And Fat Thickness Values In Line With Physical Activity

Discussion

Conclusions

Abbreviations

Declarations

References

Tables

Additional Declarations

Supplementary Files

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